Scandinavian Journal of Clinical & Laboratory Investigation

Vol. 69, No. 6, October 2009, 680686

ISSN 0036-5513 print/ISSN 1502-7686 online 2009 Informa UK Ltd. (Informa Healthcare, Taylor & Francis AS)
DOI: 10.1080/00365510902980751
Correspondence: Peng Hu, MD, Department of Pediatrics, First Afliated Hospital of Anhui Medical University, No. 218 Jixi Road, Hefei, 230022, Peoples
Republic of China. E-mail: hupeng28@yahoo.com.cn
(Received 2 September 2008; accepted 2 April 2009)
ORIGINAL ARTICLE
Characteristics of lipid metabolism under different urinary protein
excretion in children with primary nephrotic syndrome
PENG HU, LING LU, BO HU & PENG FEI DU
Department of Pediatrics, First afliated Hospital of Anhui Medical University, Hefei, Peoples Republic of China
Abstract
Hyperlipidemia (HLP), a common complication, is very prevalent in children with primary nephrotic syndrome (PNS).
HLP not only signicantly increases the cardiovascular risk in adulthood, but also accelerates the progression of renal
disease. Proteinuria as the most important pathophysiological change can reduce serum colloid osmotic pressure, which
leads to an increase in the synthesis of serum proteins including lipoproteins in the liver for export to the serum. Thus, the
severity of lipid abnormalities may correlate with the degree of proteinuria. A total of 378 children with PNS were divided
into three groups according to their urinary protein excretion (UPE), group A (50mg/kg/d proteinuria < 100mg/kg/d,
125 cases), group B (100mg/kg/d proteinuria < 200mg/kg/d, 132 cases) and group C (proteinuria 200mg/kg/d,
121 cases). In addition, 200 healthy volunteers with neither allergic nor renal disease between 3 and 14 years of age were
recruited as the control group. Fasting serum levels of lipoprotein (a) [Lp(a)], total cholesterol (TC), triglyceride (TG),
high density lipoprotein cholesterol (HDL-C), apolipoprotein A1 (apoA1), apoB, and albumin (Alb) were measured. Serum
low density lipoprotein cholesterol (LDL-C) was calculated by the Friedewald formula. As expected, when all patients were
compared with healthy children in this study, UPE and the serum concentrations of Lp(a), TC, TG, HDL-C, LDL-C, and
apoB were higher in the PNS than in the control group (p< 0.01), whereas for apoA1/B ratio the opposite was observed
(p< 0.01). Furthermore, patients in group C exhibited signicantly higher Lp(a), TC, TG, LDL-C, and apoB concentrations
than those in group A or B (p< 0.01), whereas for apoA1/B ratio the opposite was found (p< 0.01). The increase in serum
lipids was accompanied by a signicant augmented UPE in all patients (p< 0.05). More specically, positive correlations
were observed between serum levels of TC (r= + 0.80, p< 0.01), HDL (r= + 0.49, p< 0.01), LDL (r= + 0.79, p< 0.01),
ApoB (r= + 0.62, p< 0.01) and log proteinuria in group B; additionally, a negative correlation was observed between
apoA1/B ratio and log proteinuria in group B (r= 0.38, p< 0.01). However, no correlation of serum lipid proles with
UPE was determined in group A and C, respectively (p> 0.05). Serum Alb was negatively correlated with Lp(a) (r= 0.96,
p< 0.01), TC (r= 0.78, p< 0.01), TG (r= 0.78, p< 0.01), LDL-C (r= 0.88, p< 0.01), apoA1 (r= 0.26, p< 0.01), and
apoB (r= 0.71, p< 0.01), while positively correlated with apoA1/B (r= + 0.27, p< 0.01) in all nephrotic children. Further-
more, no correlation existed between serum lipid proles and Alb in group A, B and C, respectively (p> 0.05). In Conclu-
sion, secondary dyslipidemia in children with PNS is in parallel with the degree of UPE. There are diverse characteristics
of lipid metabolism under different UPE. As for the patients with medium-UPE, positive correlation between serum lipids
and proteinuria is presented.
Key Words: Nephrotic syndrome, proteinuria, hyperlipidemias, cholesterol, child
Introduction
PNS is a serious clinical syndrome characterized
by alterations of permselectivity at the glomerular cap-
illary wall, resulting in its inability to restrict the uri-
nary loss of proteins [1]. Proteinuria is not only the
typical clinical manifestation and diagnostic criteria,
but also the most substantial pathophysiological
change for PNS, which causes hypoproteinemia,
edema and hyperlipedemia (HLP) [2]. Nephrotic range
proteinuria is dened as UPE exceeding 50mg/kg
per day. The proteinuria in childhood nephrotic
syndrome (NS) is relatively selective, constituted
primarily by albumin (Alb).
HLP, a main complication of PNS, is though to
be involved in cardiovascular disease (CVD), and in
progressive glomerular damage leading to renal
failure [3,4]. Both of these hazards may prove to be
long-term factors to be considered in childhood NS
Dyslipidemia in childhood PNS 681
at 20C. Subsequent analysis of serum Lp(a) was
performed using an assay based on Sandwich
enzyme-linked immunosorbent assay (ELISA) that
is insensitive to the presence of plasminogen (RAN-
DOX, UK). Serum TC, TG, HDL-C, blood urea
nitrogen (BUN), and creatinine (Cr) were measured
by standard enzymatic method (RANDOX, UK).
Serum apoA1 and apoB were measured by immuno-
turbidimetric methods (RANDOX, UK). Serum Alb
was determined by bromocresol green method.
Serum LDL-C and estimate glomerular ltration
rate (eGFR) were calculated by the Friedewald for-
mula and the Schwartz formula respectively [8,9]. A
urine collection bag was used for the children who
couldnt control their urine emission and its reliabil-
ity has been veried by many previous studies [10,11].
Total protein from a 24-hour urine sample was deter-
mined by biuret colorimetric method (Boehringer
Mannheim Italia). All the analyses were performed in
duplicate, and the examiners were blinded to the
clinical and laboratory results.
Statistical analysis
Data are presented as mean SD and range. Because
many variables were not normally distributed,
nonparameteric statistical tests were used. Proteinuria
was analysed after logarithmic transformation for
its skewed distribution. When variables were
normally distributed, comparisons among groups
were analysed by ANOVA, Students t-test and
Chi-squared test. Correlations between variables
were assessed by linear regression. A value of p< 0.05
was considered signicant. Statistical analysis was
performed using the statistical package for social
studies SPSS version 11.5.
Results
Main clinical and biochemical characteristics of the
three nephrotic groups and controls in this study are
shown in Table I. Male/female ratio, age, body mass
index, BUN, Cr, and eGFR were almost identical
except for serum Alb in the four groups (A, B, C, and
which persists into adulthood [5]. The pathophysiology
of nephritic HLP is complex. The prevailing view is
that both hepatic synthesis of lipids and of apolipo-
proteins is increased, and that the clearance of chy-
lomicrons and very low-density lipoproteins (VLDL) is
reduced [6]. Recent studies have shown that proteinu-
ria even in the non-nephrotic range is associated with
high serum cholesterol levels [7]. However, little infor-
mation exists about the characteristics of lipid metab-
olism under different UPE in children with PNS. In
this context, we analysed the data from 378 children
suffering from PNS to address the hypothesis that
diverse characteristics of lipid metabolism may be
present according to different UPE.
Materials and methods
Subjects
The participants were 378 pediatric patients with
PNS between 2 and 14 years of age who were admitted
to the Department of Pediatrics, the First Afliated
Hospital of Anhui Medical University during the
period January 2004 to December 2006. None of
them was under steroid therapy. All patients had
nephrotic onset with proteinuria > 50mg/kg/d, hypo-
albuminemia, edema and HLP of varying degrees. All
patients were divided into three groups according to
their UPE, group A (50mg/g/d proteinuria
< 100mg/kg/d, 125 cases), group B (100mg/kg/d
proteinuria < 200mg/kg/d, 132 cases) and group C
(proteinuria 200mg/kg/d, 121 cases). The control
group consisted of 200 healthy volunteers with nei-
ther allergic nor renal disease between 3 and 14 years
of age. Main clinical and biochemical characteristics
of the four groups in this study are shown in
Table I. The study was approved by the Ethics Com-
mittee of our Medical Faculty and written informed
consent was obtained from the parents of all subjects
before study entry.
Laboratory analysis
Blood samples were collected following an overnight
fast. Serum was separated within 4h and stored
Table I. Main clinical and biochemical characteristics of the three nephrotic groups and controls.
Group Group A Group B Group C Controls p value
Cases 125 132 121 200
Male/female 86/39 91/41 85/36 132/68 NS
Age(years) 8.2 3.7 8.3 3.1 7.1 3.2 8.3 3.8 NS
Body mass index (kg/m
2
) 16.4 2.1 16.7 1.9 17.3 2.7 15.8 2.9 NS
Duration of disease (d) 10 1.2 11 1.6 10 1.5 NS
Alb (g/L) 26.3 2.8 15.9 1.2 12.1 1.4 42.3 4.7 0
BUN (mol/L) 4.7 0.7 4.7 1.1 4.9 1.3 4.4 0.9 NS
Cr (mol/L) 42.5 3.6 43.7 2.8 45.3 4.6 39.7 5.4 NS
eGFR [ml/(min.1.73m
2
)] 154.2 12.1 151.4 18.5 148.7 17.6 161.0 15.3 NS
NS, Not signicant.
682 P. Hu et al.
Relationship between serum lipid proles and
Alb in the three nephrotic groups and all patients is
shown in Table IV and Figure 1. Serum Alb
was negatively correlated with Lp(a) (r= 0.96,
p< 0.01), TC (r= 0.78, p< 0.01), TG (r= 0.78,
p< 0.01), LDL-C (r= 0.88, p< 0.01), apoA1
(r= 0.26, p< 0.01), and apoB (r= 0.71, p< 0.01),
while positively correlated with apoA1/B (r= + 0.27,
p< 0.01) in all nephrotic children. Furthermore, no
correlation existed between serum lipid proles and
Alb in group A, B and C, respectively (p> 0.05).
Discussion
In this present study, to avoid unnecessary interventions
of the duration of disease and steroid to lipid
metabolism and UPE, 378 pediatric patients with
PNS were recruited at the rst visit to our hospital,
and none of them was under steroid therapy. All
patients had nephrotic range proteinuria, hypoalbu-
minemia, edema and HLP, and were divided
into three groups according to their UPE,
group A (50mg/kg/d proteinuria < 100mg/kg/d,
125 cases), group B (100mg/kg/d proteinuria
< 200mg/kg/d, 132 cases) and group C (proteinuria
200mg/kg/d, 121 cases). Male/female ratio, age,
body mass index, BUN, Cr, eGFR, and duration of
disease were almost identical except for serum Alb
in the three nephrotic groups (A, B, and C) (p> 0.05).
controls) (p> 0.05). Moreover, the three nephrotic
groups (A, B, and C) were homogenous in the duration
of disease (p> 0.05).
Proteinuria and serum lipid proles of the three
nephrotic groups and controls are given in Table II.
Patients in group C exhibited signicantly higher
Lp(a), TC, TG, LDL-C, and apoB concentrations
than those in group A or B (p< 0.01), whereas for
apoA1/B ratio the opposite was observed (p< 0.01).
When all patients were compared with healthy children,
UPE and the serum concentrations of Lp(a),
TC, TG, HDL-C, LDL-C, and apoB were higher
in the PNS than in the control group (p< 0.01),
whereas for apoA1/B ratio the opposite was found
also (p< 0.01).
Relationship between serum lipid proles and log
proteinuria in the three nephrotic groups and all
patients is shown in Table III and Figure 1. The
increase in serum lipids was accompanied by a
signicant augmented UPE in all patients (p< 0.05).
More specically, positive correlations were observed
between serum levels of TC (r= + 0.80, p< 0.01),
HDL (r= + 0.49, p< 0.01), LDL (r= + 0.79, p< 0.01),
ApoB (r= + 0.62, p< 0.01) and log proteinuria in
group B; additionally, negative correlation was
observed between apoA1/B ratio and log proteinuria in
group B (r= 0.38, p< 0.01). However, no correla-
tion of serum lipid proles with UPE was determined
in group A and C, respectively (p> 0.05).
Table II. Proteinuria and serum lipid proles of the three nephrotic groups and controls.
Group A (n= 125) Group B (n= 132) Group C (n= 121) All patients (n= 378) Controls (n= 200)
Proteinuria (mg/kg/d) 72.0 10.9 168.3 13.5 277.5 32.3

186.4 27.8 4.2 1.0

Lp(a) (mg/L) 373.2 37.3 836.4 31.4 851.6 41.8

647.3 33.5 367.5 23.7

TC (mmol/L) 6.6 1.4 8.3 1.9 10.1 1.6

8.4 1.7 3.9 0.4

TG (mmol/L) 1.7 0.3 1.9 0.4 2.9 0.6

2.0 0.5 0.9 0.3

HDL-C (mmol/L) 1.8 0.7 1.8 0.5 2.0 0.9 1.8 0.5 1.3 0.1

LDL-C (mmol/L) 4.4 0.8 6.0 0.9 7.2 1.3

6.4 1.1 3.1 0.4

apoA1 (g/L) 1.4 0.4 1.5 0.4 1.5 0.5 1.5 0.4 1.7 0.1
apoB (g/L) 1.0 0.3 1.2 0.3 1.6 0.4

1.4 0.5 0.7 0.3

apoA1/B 1.4 0.5 1.4 0.6 1.1 0.4

1.4 0.4 2.7 0.5

p< 0.01.
Table III. Relationship between serum lipid proles and log proteinuria.
Serum lipid proles
Group A (n= 125) Group B (n= 132) Group C (n= 121) All patients (n= 378)
r p r p r p r p
Lp(a) (mg/L) 0.18 0.24 0.08 0.67 0.11 0.40 0.83 0.00

TC (mmol/L) 0.28 0.06 0.80 0.00

0.01 0.97 0.80 0.00

TG (mmol/L) 0.10 0.53 0.28 0.12 0.05 0.68 0.77 0.00

HDL-C (mmol/L) 0.13 0.39 0.49 0.00

0.04 0.73 0.20 0.02

LDL-C (mmol/L) 0.27 0.07 0.79 0.00

0.07 0.60 0.83 0.00

apoA1 (g/L) 0.23 0.13 0.06 0.76 0.06 0.63 0.19 0.03

apoB (g/L) 0.15 0.32 0.62 0.00

0.04 0.76 0.70 0.00

apoA1/B 0.09 0.57 0.38 0.00

0.09 0.45 0.23 0.01

p< 0.01,

p< 0.05.
Dyslipidemia in childhood PNS 683
900
800
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0 10 100
Log proteinuria change
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)

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(D)
Figure 1. Relationship between serum lipid proles and log proteinuria. A total of 378 children with PNS were divided into three groups
according to their UPE, group 1 (50mg/kg/d proteinuria < 100mg/kg/d, 125 cases; ), group 2 (100mg/kg/d proteinuria < 200mg/kg/d,
132 cases; g) and group 3 (proteinuria 200mg/kg/d, 121 cases; ). Linear regression was undertaken to elucidate the relationship
between serum lipid proles and log proteinuria. The increase in serum lipids was accompanied by a signicant augmented UPE in all
patients (p< 0.05). More specically, positive correlations were observed between serum levels of TC (r= + 0.80, p< 0.01; Figure 1B),
HDL (r= + 0.49, p< 0.01; Figure 1C), LDL (r= + 0.79, p< 0.01; Figure 1E), ApoB (r= + 0.62, p< 0.01; Figure 1G) and log proteinuria
in group 2; additionally, negative correlation was observed between apoA1/B ratio and log proteinuria in group 2 (r= 0.38, p< 0.01; Figure 1H).
However, no correlation of serum lipid proles with UPE was determined in group 1 and 3, respectively (p> 0.05).
In addition, 200 healthy volunteers with neither
allergic nor renal disease between 3 and 14 years of
age were recruited as the control group.
As expected, when all patients were compared
with healthy children in this study, UPE and the
serum concentrations of Lp(a), TC, TG, HDL-C,
LDL-C, and apoB were higher in the PNS than in
the control group (p< 0.01), whereas for apoA1/B
ratio the opposite was observed (p< 0.01), which
may be correlated with the report from Nanjing,
China [12]. Furthermore, our results also demonstrated
that patients in group C exhibited signicantly higher
Lp(a), TC, TG, LDL-C, and apoB concentrations
than did in group A or B with the aggravation of
proteinuria. Therefore, lipid abnormalities may be in
parallel with the degree of UPE.
It is true that the increase in serum lipids was
accompanied by a signicant augmented UPE
(p< 0.05), when linear regression analysis between
serum lipids and log proteinuria was undertaken in all
patients. Similar to our study, Khanna et al. [13] found
that the severity of proteinuria correlated positively
with serum cholesterol (r= + 0.620) and with serum
triglyceride (r= + 0.604) in 30 patients with NS.
However, the reports from Korea and Thailand exhibited
adverse results [14,15]. The possible mechanism for
these controversial comments may be other factors,
such as renal function impairment, insulin resistance
684 P. Hu et al.
Figure 1. Relationship between serum lipid proles and log proteinuria. A total of 378 children with PNS were divided into three groups
according to their UPE, group 1 (50mg/kg/d proteinuria< 100mg/kg/d, 125 cases; ), group 2 (100mg/kg/d proteinuria < 200mg/kg/d,
132 cases; g) and group 3 (proteinuria 200mg/kg/d, 121cases; ). Linear regression was undertaken to elucidate the relationship between
serum lipid proles and log proteinuria. The increase in serum lipids was accompanied by a signicant augmented UPE in all patients
(p< 0.05). More specically, positive correlations were observed between serum levels of TC (r= + 0.80, p< 0.01; Figure1B), HDL
(r= + 0.49, p< 0.01; Figure 1C), LDL (r= + 0.79, p< 0.01; Figure 1E), ApoB (r= + 0.62, p< 0.01; Figure 1G) and log proteinuria in
group 2; additionally, negative correlation was observed between apoA1/B ratio and log proteinuria in group 2 (r= 0.38, p< 0.01; Figure 1H).
However, no correlation of serum lipid proles with UPE was determined in group 1 and 3, respectively (p> 0.05) (continued).
9
8
7
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o
B

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/
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2
1
(G) 4.0
3.5
3.0
2.5
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A
p
o
A
1
/
B
3
Group
2
1
(H)
and diabetes frequently coincide with proteinuria,
and therefore also contribute to dyslipidemia [16].
Since all patients in the present study were in
primary conditions, the major factor inuencing the
association between lipid metabolism and UPE may
be focused on renal function status.
In these circumstances, we classied the severity
level of glomerular impairment based on proteinuria.
More specically, positive correlations were observed
between serum levels of TC (r= + 0.80, p< 0.01),
HDL (r= + 0.49, p< 0.01), LDL (r= + 0.79, p< 0.01),
ApoB (r= + 0.62, p< 0.01) and log proteinuria in
group B. There were also slight tendencies of positive
correlations between TC (r= + 0.28, p= 0.06),
LDL-C (r= + 0.27, p= 0.07) and log proteinuria in
group A, but no signicances were found. We specu-
lated it might be not severe enough for the decrease
of serum colloid osmotic pressure in group A, thus, the
compensatory synthesis of serum lipoproteins in liver
was not up-regulated according to UPE proportionally.
With this assumption, signicant correlation should
be presented in patients undergoing heavy proteinuria.
However, present study showed no correlation
between serum lipid proles and UPE was observed
in group C. Although the compensatory synthesis of
lipoproteins operated sufciently in this condition,
structural damage to glomerular lter in group C
might be more severe than that in former groups,
Dyslipidemia in childhood PNS 685
In conclusion, the present study indicated that
secondary dyslipidemia in children with PNS is
in parallel with the degree of UPE. There are
diverse characteristics of lipid metabolism under
different UPE. We consider that proteinuria=
100mg/kg/d may be the threshold stimulating the
hepatic synthesis of lipoproteins in patients with
PNS. Severity of HLP is accompanied by an increase
of UPE proportionally above this point. However,
the correlation is not presented until proteinuria
exceeding 200mg/kg/d.
Acknowledgements
This study was supported by Post-Doctoral Foundation
of Anhui Medical University. The authors would
like to gratefully acknowledge the most helpful
comments on this paper received from Professor
Yuan Han Qin, Department of Pediatrics, The
First Afliated Hospital of Guangxi Medical
University, Nanning.
Declaration of interest: The authors report no
conicts of interest. The authors alone are responsible
for the content and writing of the paper.
Abbreviations
HLP Hyperlipidemia
PNS Primary nephrotic syndrome
UPE Urinary protein excretion
TP Total protein
Lp(a) Lipoprotein (a)
TC Total cholesterol
TG Triglyceride
HDL-C High density lipoprotein
cholesterol
LDL-C Low density lipoprotein
cholesterol
ApoA1 Apolipoprotein A1
CVD Cardiovascular disease
VLDL Very low-density lipoprotein.
allowing many giant lipoproteins to escape into the
urine [17].
PNS is a prevalent glomerular disease during
childhood. Estimates on the annual incidence range
from 2~7 per 100,000 children, and prevalence from
12~16 per 100,000 [1]. The clinical manifestations of
childhood PNS include proteinuria, hypoproteinemia,
edema and HLP. Among them, proteinuria is the
most signicant pathophysiological change. Any factor
destroying the molecular or electrostatic barrier of
the glomerular lter can lead to proteins from the
blood escaping into the urine, which is a substantial
trigger at the onset of lipid abnormalities. First,
proteinuria has been found to be associated with
decreased post-heparin lipoprotein lipase and
increased hepatic lipase activities, which in turn
favors increased serum VLDL and LDL levels respec-
tively [18]. Second, proteinuria has been found to be
associated with a qualitative shift of LDL to the
small, dense variety, which has a lower afnity for the
LDL-receptor, resulting in its decreased serum
clearance [19]. Third, proteinuria has been associated
with elevated serum levels of inammatory markers
and cytokines, due to the underlying endothelial
damage [20]. These inammatory cytokines can
stimulate hepatic LDL-receptor gene expression and
function, resulting in hypercholesterolemia [21].
Fourth, proteinuria has been found to be associated
with fasting hyperinsulinemia, a major risk factor for
HLP [22]. Finally, animal models have demonstrated
that proteinuria can cause an up-regulation of
3-hydroxy-3-methylglutaryl-coenzyme A reductase
and down-regulation of cholesterol 7a-hydroxylase,
the rate-limiting steps in cholesterol biosynthesis and
catabolism respectively [23]. As for our study, the
negative correlation between serum lipid proles and
Alb in all nephrotic children supported indirectly the
above views that secondary hypoproteinemia might
accelerate the onset of lipid abnormalities. However, no
correlation existed between serum lipid proles and
Alb in group A, B and C. Therefore, further studies
should be warranted to elucidate these differences in
the near future.
Table IV. Relationship between serum lipid proles and Alb.
Serum lipid
proles
Group A (n= 125) Group B (n= 132) Group C (n= 121) All patients (n= 378)
r p r p r p r p
Lp(a) (mg/L) 0.11 0.49 0.10 0.58 0.13 0.32 0.96 0.00

TC (mmol/L) 0.01 0.99 0.16 0.37 0.12 0.36 0.78 0.00

TG (mmol/L) 0.26 0.08 0.07 0.69 0.07 0.58 0.78 0.00

HDL-C
(mmol/L)
0.05 0.72 0.23 0.19 0.21 0.09 0.15 0.07
LDL-C
(mmol/L)
0.10 0.52 0.11 0.53 0.06 0.61 0.88 0.00

apoA1 (g/L) 0.07 0.64 0.09 0.61 0.12 0.35 0.26 0.00

apoB (g/L) 0.12 0.43 0.06 0.75 0.10 0.43 0.71 0.00

apoA1/B 0.14 0.36 0.16 0.38 0.02 0.86 0.27 0.00

p< 0.01.
686 P. Hu et al.
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